The human brain comprises approximately 2% of the total body weight, yet it consumes 20% of the body’s oxygen [1, 2]. The basis of life phenomenon is the energy material ATP generated in a cell, while oxygen (O₂) is essential for the continued production of ATP. A few minutes of ischemia or hypoxia can lead to irreversible damage or even death of brain tissue [3]. The supply of O₂ to cells is through breathing, which transports inhaled air containing O₂ into the alveoli within the lungs, where O₂ enters the blood through gas exchange and is transported throughout the body by the arterial blood. O₂ in the capillaries is exchanged with the tissues again, to then be taken up by the cells. The majority of O₂ molecules in the blood are reversibly bound to oxyhemoglobin (HbO₂) in red blood cells, with a fraction dissolved in the plasma. When the brain is thinking, a certain area of the cerebral cortex is activated to complete the corresponding thoughts. At this time, the HbO₂ in the cortex of this area will change, with the degree of change reflecting the intensity of regional activation [4, 5]. Therefore, HbO₂ is a critical indicator of brain tissue activity and function and its regulation is essential for maintenance of normal wakefulness and cognitive function [6, 7]. Investigating changes in HbO₂ metabolism in healthy individuals can contribute to the understanding of spontaneous alterations in neural activity and responses to stimuli during brain development, maturation and aging processes [8, 9]. Moreover, HbO₂ holds significant implications for the mechanisms underlying neurological disorders such as cerebrovascular disease, mental illness and neurodegenerative disease.

Different studies have presented varying perspectives on HbO₂ metabolism during the aging process. Some investigators argue that HbO₂ metabolism decreases with age, possibly due to continuous low perfusion and oxygen supply resulting from atherosclerosis or age-related cell loss (manifested as reduced gray matter volume) or changes in cellular function (manifested as decreased oxygen utilization) [10, 11]. Alternatively, it has been suggested that despite progressive atrophy of brain structure with age, brain function remains relatively stable for an extended period [12, 13]. This implies a complex relationship between aging and HbO₂ metabolism [14]. Compared to younger adults, brain activation levels in certain regions of older adult brain tend to decrease, often accompanied by increased activation in other areas. Here, the hypothesis is that older individuals compensate for age-related neural changes by recruiting additional neural circuits or utilizing alternative pathways [15]. Since motor and cognitive tasks require the delivery of adequate oxygen and glucose to specific areas of the brain, it is thought that blood flow to specific areas should be related to enhanced metabolic activity in those areas performing a task [16]. However, this process depends on complex and poorly understood brain vascular regulation mechanisms which may change with aging and disease. A common explanation for the mismatch between cerebral blood flow and oxygen consumption during neuronal excitation is that blood flow increases beyond oxygen consumption to compensate for the depletion of oxygen reserves in brain mitochondria [17].

Aging is associated with structural and functional alterations in the brain. Consequently, it is important to explore strategies that harness the brain’s inherent plasticity and adaptability and employ continuous training methods to reshape brain function [18, 19]. Thus, individuals with impaired brain function can improve and reshape that function through continuous motor training. Currently, commonly used clinical motor controls include active, passive and imagined movements [20]. Active movements require individuals to have some degree of voluntary motor ability and are suited to late-stage recovery. In passive movement, individuals do not need to actively participate, as the entire process is carried out by therapists or therapeutic equipment, making it ideal for early-stage brain injury patients with limited motor function. Imagined movement involves patients mentally simulating actions without producing actual limb movements, making it suitable for brain injury patients with impaired motor function [21, 22]. Combined with the previous research results on the brain activation characteristics of these three motor tasks, the regions of interest (ROIs) in this study are primary somatosensory cortex (PSC), primary motor cortex (PMC), supplementary motor cortex (SMC), prefrontal cortex (PFC) and dorsolateral prefrontal cortex (DLPFC) [23, 24].

Functional near-infrared spectroscopy (fNIRS) is based on a neurovascular coupling mechanism, where local changes in brain functional activity lead to corresponding alterations in local cerebral blood flow [25, 26]. Oxygenated and deoxygenated hemoglobin in the cerebral cortex blood vessels absorb near-infrared light to varying degrees, causing near-infrared light attenuation. By analyzing the correlation between light attenuation and changes in chromophore concentration in the tissue, fNIRS can quantitatively measure changes in HbO₂ concentration in brain tissue, thus reflecting the level of brain activity [27, 28]. fNIRS provides real-time monitoring of HbO₂ metabolic levels. It is portable, easy to operate and meets the requirements of spatiotemporal resolution of brain function research, making it highly valuable and widely applicable in this field of research [29].

Batula et al. [30] used fNIRS to compare the brain activation levels of motor execution and motor imagery in the upper and lower limbs and found that motor execution activated motor areas to a greater extent than motor imagery and that the differences in the upper limbs were more obvious than those of the lower limbs. Holtzer et al. [31] used fNIRS to compare changes in cerebral oxygenation of the PFC during walking and walking while talking (dual-task) in older and younger adults and found that oxygenation levels were increased in the PFC during walking while talking when compared to only walking. Additionally, the authors found that this increase was greater in younger compared to older adults [31]. Zhang et al. [32] used fNIRS to explore age-related changes in cerebral cortex activation during finger-to-thumb opposition movement and found that the average beta values of the left and right PFC in an older group were significantly higher than for those in a younger group. Similarly to Holtzer et al. [31], some have found that older individuals demonstrate smaller changes in cerebral oxygenation during finger tapping when compared to younger individuals, which is consistent with the lower voxel activation observed in functional magnetic resonance imaging (fMRI) [33, 34]. Taken together, existing evidence on age-related differences in cerebral oxygenation suggest that younger adults demonstrate greater cerebral oxygenation during motor tasks and findings seem to vary based on the type of motor condition studied.

Here, the aim was to evaluate HbO₂ changes in five areas of the cerebral cortex (PSC, PMC, SMC, PFC and DLPFC) in younger and older adults that completed three different motor conditions (motor imagery, motor execution and motor passivity).

As mentioned above, the use of fNIRS to examine age-related differences in cerebral oxygenation in different motor control conditions is not new. A unique aspect of this study was the evaluation of multiple motor control conditions (motor execution, motor passivity and motor imagery) and targeting the following ROIs: PSC, PMC, SMC, PFC and DLPFC. Also, while there is a large literature on walking and age-differences in fNIRS [35, 36], less is known concerning elbow flexion and multiple motor conditions. However, upper limbs account for 60% of the body’s total body functions and have a direct impact on the quality of life. The elbow flexion–extension movement is intrinsic to many daily activities such as tooth brushing, face washing and eating. No previous study has reported age-related change in elbow flexion and multiple motor modes, although this activity is common in daily life. Therefore, this study used an elbow flexion task to gain a deeper understanding of the role and significance of HbO₂ metabolism and its association with the aging process. Specifically, the following hypothesis was evaluated: HbO₂ levels in different brain regions under different motor control conditions is influenced by age.

This study used fNIRS to investigate the characteristics of and differences between younger and older adults in HbO₂ level during motor execution, motor passivity and motor imagery processes. During the motor execution task, younger adults presented greater activation than older younger adults in cortex area right PMC, left PMC, right PFC, left PFC, left PSC, left SMC and left DLPFC, these brain regions being strongly associated with motor execution [43, 44, 45]. Andrews-Hanna et al. [46], found that compared to healthy younger adults, older adults show weaker levels of brain activation and perform poorly in various cognitive domains such as processing speed, memory and executive functions. They concluded that the age-related coordinated disorder of large-scale brain systems leads to cognitive decline. It is also not ruled out that with aging, the reduction in gray matter volume reduces activity in brain regions directly related to executive function [47]. Healthy brain aging can lead to sensory-motor cortex integration disorders [48] and the reduced level of neuronal metabolism is associated with an associated motor decline [49].

During the motor passivity task, younger adults presented greater activation than older adults in cortex areas: right PMC, left PMC, left PSC and left SMC and no significant differences were found in cortex areas: right PFC, left SMC and left DLPFC. This may be related to the characteristics of the motor task. Loibl et al. [50] found that the differences in motor passivity between the older and younger adults were related to the complexity of the motor tasks. When performing a simple wrist flexion task, ipsilateral PMC and SMC activation increased significantly in older adults, but when performing a complex force grip task, contralateral PSC and PMC activation were more significant in younger adults. However, the main activation areas were SMC, PMC and PSC [51], which showed similar activation areas found to the results reported here.

Simultaneously, during the motor imagery task, younger adults presented greater activation than older younger adults in cortex areas: right PFC, left PFC, left PSC, right DLPFC and left DLPFC, but no significant differences were found in the remaining brain regions. Motor imagery is an advanced type of brain thought activity and there is no consensus on which brain areas cause activation. This may be related to the different experimental methods and the complexity of the designed motor imagery task [52, 53]. However, the small activation effect of motor imagery on PMC did not reflect significant differences, which is consistent with other studies [54, 55].

According to the results reported here, it is not difficult to find that three motor control conditions examined activated specific brain regions and that there were age-related differences in HbO₂ level; with an older group exhibiting lower HbO₂ levels when compared to a younger group. Research reports have indicated that brain blood flow in older people undergoes changes when compared to younger individuals [56, 57]. Positron emission tomography and single-photon emission computed tomography scans have shown that local brain blood flow in the association cortex and the edge cortex decreases with age [57, 58]. Furthermore, fMRI studies have revealed that, when compared to younger individuals, older individuals exhibited fewer activated voxels during motor tasks, simple reaction time tasks and visual stimulus activation [59, 60]. Additionally, Hock et al. [56] demonstrated through fNIRS that older individuals exhibit less increase in oxygenated hemoglobin and total hemoglobin in the dorsolateral prefrontal cortex during cognitive tasks when compared to younger individuals. Hogstrom et al. [61], found that cortex area decreases with age and this process is nonlinear. The results presented here show different motor control conditions are associated with different HbO₂, which may be related to motor control intensity. Therefore, different motor controls have different HbO₂ levels and undergo different changes with age.

HbO₂ metabolism provides a direct in vivo measurement tool for assessing neuronal metabolism and biological activity, reflecting neuronal activity in normal resting, activated, or pathological states [62]. HbO₂ metabolism is crucial in the normal aging process. Consistent with numerous previous research findings, this study also observed a falling trend in HbO₂ level with age. In theory, the decrease in HbO₂ metabolism with age may be due to structural changes. Micro anatomical changes in the cortex during normal aging include reduced synaptic density, decreased neuronal density and a decrease in average neuron size, any of which could reduce local metabolic demand, leading to the observed reduction in HbO₂ levels [63, 64, 65].

It is worth noting that age-related changes in blood oxygenation have previously been reported. Ances et al. [66] noted a decrease in HbO₂ level at rest but a slight increase in oxygen extraction rate with age. Furthermore, Hock et al. [56] found a significant reduction in HbO₂ measured by near-infrared spectroscopy during cognitive tasks in older individuals. This finding suggests that the coupling between oxygenation and neuronal activation has changed and is consistent with the reduced blood oxygen level dependent response observed in the present study. Given the complex interplay between neuronal activation and oxygenation, the findings reported here may represent reduced neuronal activation and reduced vascular responses to different motor control conditions in older individuals.

As fNIRS is a relatively new method, it is important to consider both its advantages and limitations. Importantly, in the fNIRS method implemented here, it was not possible to obtain an absolute baseline HbO₂ concentration. This would require accurate quantification of the path-length of near-infrared light in brain tissue for each wavelength obtained for every observation. Since absolute baseline values are unknown, measurements are limited to relative changes in absolute concentration. Some might argue that brain volume in the studied older individuals is smaller than in younger individuals due to brain atrophy with aging. However, brain atrophy data measured by computed tomography in adult brains indicate only mild atrophy between the ages of 20 and 60, with significant atrophy only occurring subsequently [67]. Given that the average age of the older participants in this study was 60 years, this group may only exhibit mild atrophy compared to the younger group. It is also important to note that channel placement affect.

HbO₂ level and these levels vary if the angular position of optodes change [68]. To minimize the influence of different optodes, identical positions were selected in each subject. HbO₂ levels in the adult head remain constant once the optode distance exceeds 2.5 cm. In this study, the optode separation was three centimeters.

Analyzing the HbO₂ changes during different motor control conditions further helps understand the relationship between changes in motor control function during both the aging process and oxygen metabolism. In the future, a more in-depth exploration of HbO₂ changes in different contexts should be conducted in the presence of different stimuli such as drugs, cognitive training and transcranial direct current stimulation. This will lay a foundation for disease research. Additionally, fNIRS can be combined with other methods such as magnetoencephalography and electroencephalography to assess neurological function [69]. Despite drawbacks in its current implementation, such as spatial resolution limitations and quantitative uncertainty due to the absence of precise measurement capabilities for optical path lengths, fNIRS still holds the potential to provide non-invasive assessment of cerebral HbO₂, offering information in real-time at the bedside that no other non-invasive methods can currently provide.

This study provided evidence that HbO₂ levels are different in the primary and association cortices during different motor control conditions in young and older adults. HbO₂ levels in different brain regions under different motor control conditions can be influenced by age.

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

JL and CW contributed to conception and design. DY performed the experiments. ZY analyzed the data. DY wrote the paper. All authors contributed to editorial changes in the manuscript. All authors read and approved the final manuscript. All authors have participated sufficiently in the work and agreed to be accountable for all aspects of the work.

The present research was approved by the Biomedical Research Ethics Committee of the Second Affiliated Hospital of Nanchang University (BR/AFISG-04/1.0). After a complete description of the study, written informed consent was obtained from all patients or their families/legal guardians.

We thank two anonymous reviewers for their comments and suggestions which helped improve the manuscript.

This research was supported by Project of the Science and Technology Department of Jiangxi Province, China (20224ABC03A02).

The authors declare no conflict of interest.